Abstract
Flagellar beating drives sperm through the female reproductive tract and is vital for reproduction. Flagellar waves are generated by thousands of asymmetric molecular components; yet, paradoxically, forward swimming arises via symmetric side-to-side flagellar movement. This led to the preponderance of symmetric flagellar control hypotheses. However, molecular asymmetries must still dictate the flagellum and be manifested in the beat. Here, we reconcile molecular and microscopic observations, reconnecting structure to function, by showing that human sperm uses asymmetric and anisotropic controls to swim. High-speed three-dimensional (3D) microscopy revealed two coactive transversal controls: An asymmetric traveling wave creates a one-sided stroke, and a pulsating standing wave rotates the sperm to move equally on all sides. Symmetry is thus achieved through asymmetry, creating the optical illusion of bilateral symmetry in 2D microscopy. This shows that the sperm flagellum is asymmetrically controlled and anisotropically regularized by fast-signal transduction. This enables the sperm to swim forward.
Highlights
The coordinated motion of eukaryotic cilia and flagella is the archetype of spontaneous wave generation bridging molecular and microscopic scales in nature [1]
The combined rolling and translation motion of the sperm flagellum leads to helical trajectories of the mid-flagellar point with conserved chirality
We used high-precision 3D video microscopy to resolve the rapid movement of the human flagellum in 3D
Summary
The coordinated motion of eukaryotic cilia and flagella is the archetype of spontaneous wave generation bridging molecular and microscopic scales in nature [1]. Human sperm have been postulated to swim forward by moving their flagellum symmetrically from side-to-side [2,3,4,5,6,7,8] This perception of symmetry has not changed since Leeuwenhoek’s first observations in the 17th century (Fig. 1). This led to symmetric idealizations of the waveform in three dimensions (3D), often perceived as a conical helix, similar to a widening corkscrew. This appeared to explain, for example, the observed head spinning and helical trajectories with conserved chirality in free-swimming spermatozoa [4, 9,10,11,12,13,14], whereas our understanding of the human sperm beating has been critically limited to 2D microscopy. 2D observations of waveform symmetry have led researchers to infer symmetric control hypotheses for the spontaneous wave generation in flagella [2, 3, 15,16,17,18,19,20,21,22,23,24], from the tug of war to curvature control, sliding, and the geometric-clutch hypotheses [15,16,17,18, 21, 22, 24]
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